The two-domain tree of life is linked to a new root for the Archaea

Abstract

One of the most fundamental questions in evolutionary biology is the origin of the lineage leading to eukaryotes. Recent phylogenomic analyses have indicated an emergence of eukaryotes from within the radiation of modern Archaea and specifically from a group comprising Thaumarchaeota/"Aigarchaeota" (candidate phylum)/ Crenarchaeota/Korarchaeota (TACK). Despite their major implications, these studies were all based on the reconstruction of universal trees and left the exact placement of eukaryotes with respect to the TACK lineage unclear. Here we have applied an original two-step approach that involves the separate analysis of markers shared between Archaea and eukaryotes and between Archaea and Bacteria. This strategy allowed us to use a larger number of markers and greater taxonomic coverage, obtain high-quality alignments, and alleviate tree reconstruction artifacts potentially introduced when analyzing the three domains simultaneously. Our results robustly indicate a sister relationship of eukaryotes with the TACK superphylum that is strongly associated with a distinct root of the Archaea that lies within the Euryarchaeota, challenging the traditional topology of the archaeal tree. Therefore, if we are to embrace an archaeal origin for eukaryotes, our view of the evolution of the third domain of life will have to be profoundly reconsidered, as will many areas of investigation aimed at inferring ancestral characteristics of early life and Earth. methanogenesis | Tree of Life | ancient evolution | site-heterogeneous model | archaeal phylogeny A s was suggested by a few early phylogenetic analyses (1-3), over the past five years a number of universal trees of life rooted on the branch leading to Bacteria have supported an emergence of eukaryotes from within the radiation of modern Archaea (4-11), with a specific link to a group comprising Thaumarchaeota/"Aigarchaeota" (candidate phylum)/Crenarchaeota/Korarchaeota (the TACK superphylum) (5). This finding has very important consequences, because it clearly defines that an organism endowed with characteristics of a modern archaeon was the starting point for the process of eukaryogenesis (12, 13). Although these analyses used sophisticated approaches, they were all based on the reconstruction of universal trees of life and a restricted taxonomic sampling, in particular for the bacterial outgroup. Moreover, these studies have left the precise relationship of eukaryotes with the TACK lineages unclear (10) and showed intradomain phylogenies that were only partially resolved and often inconsistent between different analyses and with well-established relationships. In fact, analyzing the three domains at once reduces the number of markers and unambiguously aligned positions that can be used for phylogenetic reconstruction and may produce artifacts because of the very large interdomain distances (14). Furthermore, the inclusion of very fast-evolving lineages may distort the phylogeny within each domain and bias the inference of interdomain relationships. Such is the case,...

Early Microbial Evolution: The Age of Anaerobes

“…Jim Lake (1988) had subjected the rRNA data to more sophisticated analyses and found that eukaryotic cytosolic ribosomes branch within the spectrum of archaeal diversity, not as sisters to them. Twenty years later, using ribosomal protein sequence data, not just the rRNA, Cox et al (2008) obtained a similar result, and now most of the trees we see of late that link the cytosolic ribosomes of eukaryotes to prokaryotic homologs have the eukaryotes branching within the archaea, not as sisters to them (Williams et al 2013, Williams andEmbley 2014;Raymann et al 2015;Spang et al 2015). That indicates that the host lineage that acquired the mitochondrion at eukaryote origin was an archaeon, as some of us have been suggesting for some time (Martin and Mül-ler 1998;Martin et al 2001).…”

“…That makes good sense in light of the methanogenic ancestry of archaea suggested by comparative physiology (Decker et al 1970), by geochemistry (Sousa and Martin 2014), and by ribosomal phylogeny (Raymann et al 2015). Phylogenetic trees, physiology, and geochemistry will continue to enrich our understanding of evolution within archaea, and help to identify the nature of genes acquired in the course of those transitions.…”

“…Anaerobic autotrophs would be ideal, in our view, but anaerobes are probably a must. That is happening among the archaea, where the new root reported by Raymann et al (2015) puts methanogens at the base of the archaeal tree. In bacterial phylogenies, sometimes clostridia (firmicutes) tend to go deep (Table 1), but only time will tell how trees will depict early evolution or deep branching lineages a few years from now, especially as environmental sequences (Rinke et al 2013) come increasingly into play.…”

“…The reason is that one of us reported the first concatenated trees using that specific data set 15 years ago (Hansmann and Martin 2000), overlooked in Ciccarelli et al's (2006) "automated" procedure to produce a tree of life that found the same proteins, and it was immediately apparent that there are many, many saturated sites in the alignments of that data set, and that if we start removing the saturated sites or those lacking observable sequence conservation then we obtain different topologies. Investigators are still using such site stripping approaches today (Petitjean et al 2015;Raymann et al 2015), sometimes pruning alignments by hand (Spang et al 2015), but the problem is that there is no good justification for when to stop excluding either genes or sites, one just gets different likelihoods. With large concatenated data sets, the results become dependent on which fraction of the data one retains in the alignment and which model one uses to infer the tree, as seen in the Petitjean et al (2015) analysis in which the archaeal root changed from being within methanogenic lineages to being between the euryarchaeota and TACK groups after pruning.…”

Eukaryotes first: how could that be?

“…This will require a taxon-rich, diverse, rooted and uncontroversial deep archaeal tree, in which Eukarya are securely located [46]. Consensus will be difficult to achieve, however.…”